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The Journal of Neuroscience, May 7, 2008, 28(19):5127-5138; doi:10.1523/JNEUROSCI.0319-08.2008

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Behavioral/Systems/Cognitive
Rat Orbitofrontal Cortex Separately Encodes Response and Outcome Information during Performance of Goal-Directed Behavior

Tomoyuki Furuyashiki, Peter C. Holland, and Michela Gallagher

Department of Psychological and Brain Sciences, Johns Hopkins University, Baltimore, Maryland 21218

Correspondence should be addressed to either Dr. Tomoyuki Furuyashiki or Dr. Michela Gallagher, Department of Psychological and Brain Sciences, Johns Hopkins University, Baltimore, MD 21218. Email: tfuruya{at}mfour.med.kyoto-u.ac.jp or Email: michela{at}jhu.edu

Orbitofrontal cortex (OFC) neurons encode rewards and the cues that predict them, providing a neural substrate for outcome expectancy, an important component of goal-directed behavior in animals and humans. Here, we recorded and analyzed single units from rat lateral OFC during performance of a task in which the encoding of an expected rewarding outcome could be isolated from the response made in obtaining it. We found concurrent encoding of the expected outcome and the behavioral response in mostly separate populations of OFC units, in each phase of task performance: odor sampling, behavioral response, and waiting during the delay before reward delivery. Population analyses showed that outcome encoding broadly spanned across each behavioral phase, whereas response-selective firings were time-locked to the behavioral events, especially the completion of the behavioral response. A significant subset of outcome-selective units maintained selective firings from either odor sampling or response initiation until reward delivery. In contrast, response-selective units typically showed transient activation time locked to the behavioral events and were less likely to maintain selective firings across behavioral phases than outcome-selective units. These data demonstrate a broader role of OFC information processing in goal-directed behavior, beyond its widely recognized role in outcome expectancy.

Key words: orbitofrontal cortex; orbital cortex; expected reward; behavioral response; associative learning; goal-directed behavior

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Received Jan. 23, 2008; revised April 7, 2008; accepted April 9, 2008.

Correspondence should be addressed to either Dr. Tomoyuki Furuyashiki or Dr. Michela Gallagher, Department of Psychological and Brain Sciences, Johns Hopkins University, Baltimore, MD 21218. Email: tfuruya{at}mfour.med.kyoto-u.ac.jp or Email: michela{at}jhu.edu

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